Skip to main content

Advertisement

SpringerLink
Log in

Disuse of the musculo-skeletal system in space and on earth

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Muscle mass and strength are well known to decline in response to actual and simulated microgravity exposure. However, despite the considerable knowledge gained on the physiological changes induced by spaceflight, the mechanisms of muscle atrophy and the effectiveness of in-flight countermeasures still need to be fully elucidated. The present review examines the effects and mechanisms of actual and simulated microgravity on single fibre and whole muscle structural and functional properties, protein metabolism, tendon mechanical properties, neural drive and reflex excitability. The effects of inflight countermeasures are also discussed in the light of recent advances in resistive loading techniques, in combined physical, pharmacological and nutritional interventions as well as in the development of artificial gravity systems. Emphasis has been given to the pioneering work of Pietro Enrico di Prampero in the development of artificial gravity systems and in the progress of knowledge on the limits of human muscular performance in space.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Notes

  1. Maximum unloaded shortening velocity (V 0) is estimated in isolated preparations using the so-called ‘slack’ test (Edman (1979). A contracting muscle is rapidly shortened by a known distance (at a velocity greater than V max) so that the fibres become slack and will then shorten without any external load. The time for the fibre to take up the slack and start pulling on the force transducer gives a measure of the velocity of unloaded shortening. Maximum shortening velocity (V max) is estimated from the force–velocity relationship, which in turn is determined from a series of consecutive isotonic steps. V max is defined as the intercept of the force–velocity curve with the velocity axis.

References

  • Adams GR, Hather BM, Dudley GA (1994) Effect of short-term unweighting on human skeletal muscle strength and size. Aviat Space Environ Med 65:1116–1121

    CAS  PubMed  Google Scholar 

  • Akima H, Kawakami Y, Kubo K, Sekiguchi C, Ohshima H, Miyamoto A, Fukunaga T (2000) Effect of short-duration spaceflight on thigh and leg muscle volume. Med Sci Sports Exerc 32:1743–1747

    Article  CAS  PubMed  Google Scholar 

  • Akima H, Kubo K, Imai M, Kanehisa H, Suzuki Y, Gunji A, Fukunaga T (2001) Inactivity and muscle: effect of resistance training during bed rest on muscle size in the lower limb. Acta Physiol Scand 172:269–278

    Article  CAS  PubMed  Google Scholar 

  • Akima H, Katayama K, Sato K, Ishida K, Masuda K, Takada H, Watanabe Y, Iwase S (2005) Intensive cycle training with artificial gravity maintains muscle size during bed rest. Aviat Space Environ Med 76:923–929

    PubMed  Google Scholar 

  • Alkner BA, Tesch PA (2004a) Efficacy of a gravity-independent resistance exercise device as a countermeasure to muscle atrophy during 29-day bed rest. Acta Physiol Scand 181:345–357

    Article  CAS  PubMed  Google Scholar 

  • Alkner BA, Tesch PA (2004b) Knee extensor and plantar flexor muscle size and function following 90 days of bed rest with or without resistance exercise. Eur J Appl Physiol 93:294–305

    Article  PubMed  Google Scholar 

  • Andersen JL, Mohr T, Biering-Sorensen F, Galbo H, Kjaer M (1996) Myosin heavy chain isoform transformation in single fibres from m. vastus lateralis in spinal cord injured individuals: effects of long-term functional electrical stimulation (FES). Pflugers Arch 431:513–518

    Article  CAS  PubMed  Google Scholar 

  • Antonutto G, Capelli C, Di Prampero PE (1991) Pedalling in space as a countermeasure to microgravity deconditioning. Microgravity Q 1:93–101

    Google Scholar 

  • Antonutto G, Capelli C, Girardis M, Zamparo P, di Prampero PE (1999) Effects of microgravity on maximal power of lower limbs during very short efforts in humans. J Appl Physiol 86:85–92

    CAS  PubMed  Google Scholar 

  • Apseloff G, Girten B, Walker M, Shepard DR, Krecic ME, Stern LS, Gerber N (1993) Aminohydroxybutane bisphosphonate and clenbuterol prevent bone changes and retard muscle atrophy respectively in tail-suspended rats. J Pharmacol Exp Ther 264:1071–1078

    CAS  PubMed  Google Scholar 

  • Baldwin KM, Haddad F (2001) Effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle. J Appl Physiol 90:345–357

    Article  CAS  PubMed  Google Scholar 

  • Bamman MM, Clarke MS, Feeback DL, Talmadge RJ, Stevens BR, Lieberman SA, Greenisen MC (1998) Impact of resistance exercise during bed rest on skeletal muscle sarcopenia and myosin isoform distribution. J Appl Physiol 84:157–163

    CAS  PubMed  Google Scholar 

  • Belavy DL, Miokovic T, Armbrecht G, Richardson CA, Rittweger J, Felsenberg D (2009) Differential atrophy of the lower-limb musculature during prolonged bed-rest. Eur J Appl Physiol 107:489–499

    Article  PubMed  Google Scholar 

  • Berg HE, Tesch PA (1996) Changes in muscle function in response to 10 days of lower limb unloading in humans. Acta Physiol Scand 157:63–70

    Article  CAS  PubMed  Google Scholar 

  • Berg HE, Tesch PA (1998) Force and power characteristics of a resistive exercise device for use in space. Acta Astronaut 42:219–230

    Google Scholar 

  • Berg HE, Dudley GA, Haggmark T, Ohlsen H, Tesch PA (1991) Effects of lower limb unloading on skeletal muscle mass and function in humans. J Appl Physiol 70:1882–1885

    Article  CAS  PubMed  Google Scholar 

  • Berg HE, Dudley GA, Hather B, Tesch PA (1993) Work capacity and metabolic and morphologic characteristics of the human quadriceps muscle in response to unloading. Clin Physiol 13:337–347

    Article  CAS  PubMed  Google Scholar 

  • Berg HE, Larsson L, Tesch PA (1997) Lower limb skeletal muscle function after 6 wk of bed rest. J Appl Physiol 82:182–188

    Article  CAS  PubMed  Google Scholar 

  • Berg HE, Eiken O, Miklavcic L, Mekjavic IB (2007) Hip, thigh and calf muscle atrophy and bone loss after 5-week bedrest inactivity. Eur J Appl Physiol 99:283–289

    Article  PubMed  Google Scholar 

  • Boudreau NJ, Jones PL (1999) Extracellular matrix and integrin signalling: the shape of things to come. Biochem J 339(Pt 3):481–488

    Article  CAS  PubMed  Google Scholar 

  • Brooks N, Cloutier GJ, Cadena SM, Layne JE, Nelsen CA, Freed AM, Roubenoff R, Castaneda-Sceppa C (2008) Resistance training and timed essential amino acids protect against the loss of muscle mass and strength during 28 days of bed rest and energy deficit. J Appl Physiol 105:241–248

    Article  CAS  PubMed  Google Scholar 

  • Caiozzo VJ, Baker MJ, Herrick RE, Tao M, Baldwin KM (1994) Effect of spaceflight on skeletal muscle: mechanical properties and myosin isoform content of a slow muscle. J Appl Physiol 76:1764–1773

    Article  CAS  PubMed  Google Scholar 

  • Caiozzo VJ, Haddad F, Baker MJ, Herrick RE, Prietto N, Baldwin KM (1996) Microgravity-induced transformations of myosin isoforms and contractile properties of skeletal muscle. J Appl Physiol 81:123–132

    CAS  PubMed  Google Scholar 

  • Caiozzo VJ, Haddad F, Lee S, Baker M, Paloski W, Baldwin KM (2009) Artificial gravity as a countermeasure to microgravity: a pilot study examining the effects on knee extensor and plantar flexor muscle groups. J Appl Physiol 107:39–46

    Article  CAS  PubMed  Google Scholar 

  • Caruso J, Hamill J, Yamauchi M, Mercado D, Cook T, Higginson B, O’Meara S, Elias J, Siconolfi S (2005) Albuterol aids resistance exercise in reducing unloading-induced ankle extensor strength losses. J Appl Physiol 98:1705–1711

    Article  CAS  PubMed  Google Scholar 

  • Chase GA, Grave C, Rowell LB (1966) Independence of changes in functional and performance capacities attending prolonged bed rest. Aerosp Med 37:1232–1238

    CAS  PubMed  Google Scholar 

  • Cherepakhin MA, Pervushin VI (1970) Space flight effect on the neuromuscular system of cosmonauts. Kosm Biol Aviakosm Med 4:46–49

    Google Scholar 

  • Clark BC, Fernhall B, Ploutz-Snyder LL (2006) Adaptations in human neuromuscular function following prolonged unweighting: I. Skeletal muscle contractile properties and applied ischemia efficacy. J Appl Physiol 101:256–263

    Article  PubMed  Google Scholar 

  • Clark BC, Pierce JR, Manini TM, Ploutz-Snyder LL (2007) Effect of prolonged unweighting of human skeletal muscle on neuromotor force control. Eur J Appl Physiol 100:53–62

    Article  PubMed  Google Scholar 

  • Convertino VA (1990) Physiological adaptations to weightlessness: effects on exercise and work performance. Exerc Sport Sci Rev 18:119–166

    Article  CAS  PubMed  Google Scholar 

  • Convertino VA, Doerr DF, Stein SL (1989) Changes in size and compliance of the calf after 30 days of simulated microgravity. J Appl Physiol 66:1509–1512

    CAS  PubMed  Google Scholar 

  • Criswell DS, Booth FW, DeMayo F, Schwartz RJ, Gordon SE, Fiorotto ML (1998) Overexpression of IGF-I in skeletal muscle of transgenic mice does not prevent unloading-induced atrophy. Am J Physiol 275:E373–E379

    CAS  PubMed  Google Scholar 

  • D’Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, Canepari M, Saltin B, Bottinelli R (2003) The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 552:499–511

    Article  PubMed  CAS  Google Scholar 

  • Danielsen CC, Andreassen TT (1988) Mechanical properties of rat tail tendon in relation to proximal-distal sampling position and age. J Biomech 21:207–212

    Article  CAS  PubMed  Google Scholar 

  • Davies CT, Rutherford IC, Thomas DO (1987) Electrically evoked contractions of the triceps surae during and following 21 days of voluntary leg immobilization. Eur J Appl Physiol Occup Physiol 56:306–312

    Article  CAS  PubMed  Google Scholar 

  • de Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV (2007a) Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol 583:1079–1091

    Article  PubMed  CAS  Google Scholar 

  • de Boer MD, Selby A, Atherton P, Smith K, Seynnes OR, Maganaris CN, Maffulli N, Movin T, Narici MV, Rennie MJ (2007b) The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585:241–251

    Article  PubMed  CAS  Google Scholar 

  • de Boer MD, Seynnes OR, di Prampero PE, Pisot R, Mekjavic IB, Biolo G, Narici MV (2008) Effect of 5 weeks horizontal bed rest on human muscle thickness and architecture of weight bearing and non-weight bearing muscles. Eur J Appl Physiol 104:401–407

    Article  PubMed  Google Scholar 

  • Deschenes MR, Giles JA, McCoy RW, Volek JS, Gomez AL, Kraemer WJ (2002) Neural factors account for strength decrements observed after short-term muscle unloading. Am J Physiol 282:R578–R583

    CAS  Google Scholar 

  • Desplanches D, Hoppeler H, Mayet MH, Denis C, Claassen H, Ferretti G (1998) Effects of bedrest on deltoideus muscle morphology and enzymes. Acta Physiol Scand 162:135–140

    Article  CAS  PubMed  Google Scholar 

  • di Prampero PE (2000) Cycling on Earth, in space, on the Moon. Eur J Appl Physiol 82:345–360

    Article  CAS  PubMed  Google Scholar 

  • di Prampero PE, Antonutto G (1997) Cycling in space to simulate gravity. Int J Sports Med 18(Suppl 4):S324–S326

    Article  PubMed  Google Scholar 

  • di Prampero PE, Narici MV (2003) Muscles in microgravity: from fibres to human motion. J Biomech 36:403–412

    Article  PubMed  Google Scholar 

  • di Prampero P, Lazzer S, Antonutto G (2009) Human power centrifuges on the Moon and Mars. Microgravity Sci Technol 21:209–215

    Article  Google Scholar 

  • Duchateau J (1995) Bed rest induces neural and contractile adaptations in triceps surae. Med Sci Sports Exerc 27:1581–1589

    CAS  PubMed  Google Scholar 

  • Duchateau J, Hainaut K (1987) Electrical and mechanical changes in immobilized human muscle. J Appl Physiol 62:2168–2173

    CAS  PubMed  Google Scholar 

  • Dudley GA, Duvoisin MR, Convertino VA, Buchanan P (1989) Alterations of the in vivo torque-velocity relationship of human skeletal muscle following 30 days exposure to simulated microgravity. Aviat Space Environ Med 60:659–663

    CAS  PubMed  Google Scholar 

  • Dudley GA, Duvoisin MR, Adams GR, Meyer RA, Belew AH, Buchanan P (1992) Adaptations to unilateral lower limb suspension in humans. Aviat Space Environ Med 63:678–683

    CAS  PubMed  Google Scholar 

  • Duvoisin MR, Convertino VA, Buchanan P, Gollnick PD, Dudley GA (1989) Characteristics and preliminary observations of the influence of electromyostimulation on the size and function of human skeletal muscle during 30 days of simulated microgravity. Aviat Space Environ Med 60:671–678

    CAS  PubMed  Google Scholar 

  • Edgerton VR, Roy RR (1994) Neuromuscular adaptation to actual and simulated weightlessness. Adv Space Biol Med 4:33–67

    Article  CAS  PubMed  Google Scholar 

  • Edgerton VR, Zhou MY, Ohira Y, Klitgaard H, Jiang B, Bell G, Harris B, Saltin B, Gollnick PD, Roy RR et al (1995) Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. J Appl Physiol 78:1733–1739

    CAS  PubMed  Google Scholar 

  • Edgerton VR, McCall GE, Hodgson JA, Gotto J, Goulet C, Fleischmann K, Roy RR (2001) Sensorimotor adaptations to microgravity in humans. J Exp Biol 204:3217–3224

    CAS  PubMed  Google Scholar 

  • Edman KA (1979) The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J Physiol 291:143–159

    CAS  PubMed  Google Scholar 

  • Ferrando AA, Stuart CA, Brunder DG, Hillman GR (1995) Magnetic resonance imaging quantitation of changes in muscle volume during 7 days of strict bed rest. Aviat Space Environ Med 66:976–981

    CAS  PubMed  Google Scholar 

  • Ferrando AA, Lane HW, Stuart CA, Davis-Street J, Wolfe RR (1996) Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 270:E627–E633

    CAS  PubMed  Google Scholar 

  • Ferrando AA, Tipton KD, Bamman MM, Wolfe RR (1997) Resistance exercise maintains skeletal muscle protein synthesis during bed rest. J Appl Physiol 82:807–810

    CAS  PubMed  Google Scholar 

  • Ferrando AA, Tipton KD, Doyle D, Phillips SM, Cortiella J, Wolfe RR (1998) Testosterone injection stimulates net protein synthesis but not tissue amino acid transport. Am J Physiol 275:E864–E871

    CAS  PubMed  Google Scholar 

  • Ferrando AA, Paddon-Jones D, Wolfe RR (2002) Alterations in protein metabolism during space flight and inactivity. Nutrition 18:837–841

    Article  CAS  PubMed  Google Scholar 

  • Ferretti G, Berg HE, Minetti AE, Moia C, Rampichini S, Narici MV (2001) Maximal instantaneous muscular power after prolonged bed rest in humans. J Appl Physiol 90:431–435

    CAS  PubMed  Google Scholar 

  • Ferrucci L, Guralnik JM (2003) Inflammation, hormones, and body composition at a crossroad. Am J Med 115:501–502

    Article  PubMed  Google Scholar 

  • Fitts RH, Riley DR, Widrick JJ (2000) Physiology of a microgravity environment invited review: microgravity and skeletal muscle. J Appl Physiol 89:823–839

    CAS  PubMed  Google Scholar 

  • Fitts RH, Riley DR, Widrick JJ (2001) Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol 204:3201–3208

    CAS  PubMed  Google Scholar 

  • Fitts RH, Romatowski JG, Peters JR, Paddon-Jones D, Wolfe RR, Ferrando AA (2007) The deleterious effects of bed rest on human skeletal muscle fibers are exacerbated by hypercortisolemia and ameliorated by dietary supplementation. Am J Physiol Cell Physiol 293:C313–C320

    Article  CAS  PubMed  Google Scholar 

  • Fluck M, Carson JA, Gordon SE, Ziemiecki A, Booth FW (1999) Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am J Physiol 277:C152–C162

    CAS  PubMed  Google Scholar 

  • Fluckey JD, Dupont-Versteegden EE, Montague DC, Knox M, Tesch P, Peterson CA, Gaddy-Kurten D (2002) A rat resistance exercise regimen attenuates losses of musculoskeletal mass during hindlimb suspension. Acta Physiol Scand 176:293–300

    Article  CAS  PubMed  Google Scholar 

  • Gamrin L, Berg HE, Essen P, Tesch PA, Hultman E, Garlick PJ, McNurlan MA, Wernerman J (1998) The effect of unloading on protein synthesis in human skeletal muscle. Acta Physiol Scand 163:369–377

    Article  CAS  PubMed  Google Scholar 

  • Gans C, Bock WJ (1965) The functional significance of muscle architecture—a theoretical analysis. Ergeb Anat Entwicklungsgesch 38:115–142

    CAS  PubMed  Google Scholar 

  • Gardetto PR, Schluter JM, Fitts RH (1989) Contractile function of single muscle fibers after hindlimb suspension. J Appl Physiol 66:2739–2749

    CAS  PubMed  Google Scholar 

  • Gibson JN, Halliday D, Morrison WL, Stoward PJ, Hornsby GA, Watt PW, Murdoch G, Rennie MJ (1987) Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin Sci (Lond) 72:503–509

    CAS  Google Scholar 

  • Gogia P, Schneider VS, LeBlanc AD, Krebs J, Kasson C, Pientok C (1988) Bed rest effect on extremity muscle torque in healthy men. Arch Phys Med Rehabil 69:1030–1032

    CAS  PubMed  Google Scholar 

  • Gopalakrishnan R, Genc KO, Rice AJ, Lee SM, Evans HJ, Maender CC, Ilaslan H, Cavanagh PR (2010) Muscle volume, strength, endurance, and exercise loads during 6-month missions in space. Aviat Space Environ Med 81:91–102

    Google Scholar 

  • Goubel F (1997) Changes in mechanical properties of human muscle as a result of spaceflight. Int J Sports Med 18(Suppl 4):S285–S287

    Article  PubMed  Google Scholar 

  • Greenisen MC, Edgerton VR (1994) Human capabilities in the space environment. In: Nicogossian AE, Huntoon CL, Pool SL (eds) Space physiology and medicine. Lea & Febiger, Philadelphia, PA, pp 194–210

    Google Scholar 

  • Greenleaf JE, Bernauer EM, Ertl AC, Trowbridge TS, Wade CE (1989a) Work capacity during 30 days of bed rest with isotonic and isokinetic exercise training. J Appl Physiol 67:1820–1826

    CAS  PubMed  Google Scholar 

  • Greenleaf JE, Bulbulian R, Bernauer EM, Haskell WL, Moore T (1989b) Exercise-training protocols for astronauts in microgravity. J Appl Physiol 67:2191–2204

    CAS  PubMed  Google Scholar 

  • Grogor’eva LS, Kozlovskaia IB (1987) Effect of weightlessness and hypokinesia on the velocity-strength properties of human muscles. Kosm Biol Aviakosm Med 21:27–30

    PubMed  Google Scholar 

  • Hather BM, Adams GR, Tesch PA, Dudley GA (1992) Skeletal muscle responses to lower limb suspension in humans. J Appl Physiol 72:1493–1498

    CAS  PubMed  Google Scholar 

  • Haus JM, Carrithers JA, Carroll CC, Tesch PA, Trappe TA (2007) Contractile and connective tissue protein content of human skeletal muscle: effects of 35 and 90 days of simulated microgravity and exercise countermeasures. Am J Physiol 293:R1722–R1727

    Google Scholar 

  • Hespel P, Op’t Eijnde B, Van Leemputte M, Urso B, Greenhaff PL, Labarque V, Dymarkowski S, Van Hecke P, Richter EA (2001) Oral creatine supplementation facilitates the rehabilitation of disuse atrophy and alters the expression of muscle myogenic factors in humans. J Physiol 536:625–633

    Article  CAS  PubMed  Google Scholar 

  • Hikida RS, Gollnick PD, Dudley GA, Convertino VA, Buchanan P (1989) Structural and metabolic characteristics of human skeletal muscle following 30 days of simulated microgravity. Aviat Space Environ Med 60:664–670

    CAS  PubMed  Google Scholar 

  • Hortobagyi T, Dempsey L, Fraser D, Zheng D, Hamilton G, Lambert J, Dohm L (2000) Changes in muscle strength, muscle fibre size and myofibrillar gene expression after immobilization and retraining in humans. J Physiol 524(Pt 1):293–304

    Article  CAS  PubMed  Google Scholar 

  • Jaweed MM (1994) Muscle structure and function. In: Nicogossian AE, Huntoon CL, Pool SL (eds) Space physiology and medicine. Lea & Febiger, Philadelphia, pp 317–326

  • Kakurin LI, Cherepakhin MA, Pervushin VI (1971) Effect of brief space flights on the human neuromuscular system. Kosm Biol Aviakosm Med 5:53–56

    Google Scholar 

  • Kawakami Y, Muraoka Y, Kubo K, Suzuki Y, Fukunaga T (2000) Changes in muscle size and architecture following 20 days of bed rest. J Gravit Physiol 7:53–59

    CAS  PubMed  Google Scholar 

  • Kawakami Y, Akima H, Kubo K, Muraoka Y, Hasegawa H, Kouzaki M, Imai M, Suzuki Y, Gunji A, Kanehisa H, Fukunaga T (2001) Changes in muscle size, architecture, and neural activation after 20 days of bed rest with and without resistance exercise. Eur J Appl Physiol 84:7–12

    Article  CAS  PubMed  Google Scholar 

  • Klossner S, Durieux AC, Freyssenet D, Flueck M (2009) Mechano-transduction to muscle protein synthesis is modulated by FAK. Eur J Appl Physiol 106:389–398

    Article  CAS  PubMed  Google Scholar 

  • Koryak Y (1995) Contractile properties of the human triceps surae muscle during simulated weightlessness. Eur J Appl Physiol Occup Physiol 70:344–350

    Article  CAS  PubMed  Google Scholar 

  • Koryak Y (1998) Effect of 120 days of bed-rest with and without countermeasures on the mechanical properties of the triceps surae muscle in young women. Eur J Appl Physiol Occup Physiol 78:128–135

    Article  CAS  PubMed  Google Scholar 

  • Koryak Y (1999) The effects of long-term simulated microgravity on neuromuscular performance in men and women. Eur J Appl Physiol Occup Physiol 79:168–175

    Article  CAS  PubMed  Google Scholar 

  • Koryak YU (2001) Electrically evoked and voluntary properties of the human triceps surae muscle: effects of long-term spaceflights. Acta Physiol Pharmacol Bulg 26:21–27

    CAS  PubMed  Google Scholar 

  • Kozlovskaya IB, Grigoriev AI (2004) Russian system of countermeasures on board of the International Space Station (ISS): the first results. Acta Astronaut 55:233–237

    Article  PubMed  Google Scholar 

  • Kozlovskaya IB, Kreidich Yu V, Oganov VS, Koserenko OP (1981) Pathophysiology of motor functions in prolonged manned space flights. Acta Astronaut 8:1059–1072

    Article  CAS  PubMed  Google Scholar 

  • Kubo K, Akima H, Kouzaki M, Ito M, Kawakami Y, Kanehisa H, Fukunaga T (2000) Changes in the elastic properties of tendon structures following 20 days bed-rest in humans. Eur J Appl Physiol 83:463–468

    Article  CAS  PubMed  Google Scholar 

  • Kubo K, Akima H, Ushiyama J, Tabata I, Fukuoka H, Kanehisa H, Fukunaga T (2004) Effects of 20 days of bed rest on the viscoelastic properties of tendon structures in lower limb muscles. Br J Sports Med 38:324–330

    Article  CAS  PubMed  Google Scholar 

  • Lalani R, Bhasin S, Byhower F, Tarnuzzer R, Grant M, Shen R, Asa S, Ezzat S, Gonzalez-Cadavid NF (2000) Myostatin and insulin-like growth factor-I and -II expression in the muscle of rats exposed to the microgravity environment of the NeuroLab space shuttle flight. J Endocrinol 167:417–428

    Article  CAS  PubMed  Google Scholar 

  • Lambertz D, Perot C, Kaspranski R, Goubel F (2001) Effects of long-term spaceflight on mechanical properties of muscles in humans. J Appl Physiol 90:179–188

    CAS  PubMed  Google Scholar 

  • Larsson L, Li X, Berg HE, Frontera WR (1996) Effects of removal of weight-bearing function on contractility and myosin isoform composition in single human skeletal muscle cells. Pflugers Arch 432:320–328

    Article  CAS  PubMed  Google Scholar 

  • Lazzer S, Plaino L, Antonutto G (2010) The energetics of cycling on Earth, Moon and Mars. Eur J Appl Physiol (Epub)

  • LeBlanc A, Gogia P, Schneider V, Krebs J, Schonfeld E, Evans H (1988) Calf muscle area and strength changes after five weeks of horizontal bed rest. Am J Sports Med 16:624–629

    Article  CAS  PubMed  Google Scholar 

  • LeBlanc AD, Schneider VS, Evans HJ, Pientok C, Rowe R, Spector E (1992) Regional changes in muscle mass following 17 weeks of bed rest. J Appl Physiol 73:2172–2178

    CAS  PubMed  Google Scholar 

  • LeBlanc A, Rowe R, Schneider V, Evans H, Hedrick T (1995) Regional muscle loss after short duration spaceflight. Aviat Space Environ Med 66:1151–1154

    CAS  PubMed  Google Scholar 

  • LeBlanc A, Rowe R, Evans H, West S, Shackelford L, Schneider V (1997) Muscle atrophy during long duration bed rest. Int J Sports Med 18(Suppl 4):S283–S285

    Article  PubMed  Google Scholar 

  • LeBlanc A, Lin C, Shackelford L, Sinitsyn V, Evans H, Belichenko O, Schenkman B, Kozlovskaya I, Oganov V, Bakulin A, Hedrick T, Feeback D (2000) Muscle volume, MRI relaxation times (T2), and body composition after spaceflight. J Appl Physiol 89:2158–2164

    CAS  PubMed  Google Scholar 

  • Lynch GS, Hinkle RT, Faulkner JA (2001) Force and power output of diaphragm muscle strips from mdx and control mice after clenbuterol treatment. Neuromuscul Disord 11:192–196

    Article  CAS  PubMed  Google Scholar 

  • Maltin CA, Delday MI, Watson JS, Heys SD, Nevison IM, Ritchie IK, Gibson PH (1993) Clenbuterol, a beta-adrenoceptor agonist, increases relative muscle strength in orthopaedic patients. Clin Sci (Lond) 84:651–654

    CAS  Google Scholar 

  • McDonald KS, Fitts RH (1995) Effect of hindlimb unloading on rat soleus fiber force, stiffness, and calcium sensitivity. J Appl Physiol 79:1796–1802

    CAS  PubMed  Google Scholar 

  • Milesi S, Capelli C, Denoth J, Hutchinson T, Stussi E (2000) Effects of 17 days bedrest on the maximal voluntary isometric torque and neuromuscular activation of the plantar and dorsal flexors of the ankle. Eur J Appl Physiol 82:197–205

    Article  CAS  PubMed  Google Scholar 

  • Montgomery LD (1993) Body volume changes during simulated microgravity. II: comparison of horizontal and head-down bed rest. Aviat Space Environ Med 64:899–904

    CAS  PubMed  Google Scholar 

  • Murton AJ, Constantin D, Greenhaff PL (2008) The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy. Biochim Biophys Acta 1782:730–743

    CAS  PubMed  Google Scholar 

  • Narici M, Capodaglio P (1998) Changes in muscle size and architecture in disuse atrophy. In: Capodaglio P, Narici M (eds) Muscle atrophy: disuse and disease. Le Collane della Fondazione Salvatore Maugeri, PI-ME Press, Pavia, Italy, pp 55–64

  • Narici M, Cerretelli P (1998) Changes in human muscle architecture in disuse-atrophy evaluated by ultrasound imaging. J Gravit Physiol 5:P73–P74

    CAS  PubMed  Google Scholar 

  • Narici M, Kayser B, Barattini P, Cerretelli P (2003) Effects of 17-day spaceflight on electrically evoked torque and cross-sectional area of the human triceps surae. Eur J Appl Physiol 90:275–282

    Google Scholar 

  • Ohira Y, Jiang B, Roy RR, Oganov V, Ilyina-Kakueva E, Marini JF, Edgerton VR (1992) Rat soleus muscle fiber responses to 14 days of spaceflight and hindlimb suspension. J Appl Physiol 73:51S–57S

    CAS  PubMed  Google Scholar 

  • Ohira Y, Yoshinaga T, Ohara M, Nonaka I, Yoshioka T, Yamashita-Goto K, Shenkman BS, Kozlovskaya IB, Roy RR, Edgerton VR (1999) Myonuclear domain and myosin phenotype in human soleus after bed rest with or without loading. J Appl Physiol 87:1776–1785

    CAS  PubMed  Google Scholar 

  • Paddon-Jones D, Sheffield-Moore M, Cree MG, Hewlings SJ, Aarsland A, Wolfe RR, Ferrando AA (2006) Atrophy and impaired muscle protein synthesis during prolonged inactivity and stress. J Clin Endocrinol Metab 91:4836–4841

    Article  CAS  PubMed  Google Scholar 

  • Pavy-Le Traon A, Heer M, Narici MV, Rittweger J, Vernikos J (2007) From space to Earth: advances in human physiology from 20 years of bed rest studies (1986–2006). Eur J Appl Physiol 101:143–194

    Article  CAS  PubMed  Google Scholar 

  • Payette H, Roubenoff R, Jacques PF, Dinarello CA, Wilson PW, Abad LW, Harris T (2003) Insulin-like growth factor-1 and interleukin 6 predict sarcopenia in very old community-living men and women: the Framingham Heart Study. J Am Geriatr Soc 51:1237–1243

    Article  PubMed  Google Scholar 

  • Ploutz-Snyder LL, Tesch PA, Crittenden DJ, Dudley GA (1995) Effect of unweighting on skeletal muscle use during exercise. J Appl Physiol 79:168–175

    CAS  PubMed  Google Scholar 

  • Ploutz-Snyder LL, Tesch PA, Hather BM, Dudley GA (1996) Vulnerability to dysfunction and muscle injury after unloading. Arch Phys Med Rehabil 77:773–777

    Article  CAS  PubMed  Google Scholar 

  • Prockop DJ, Kivirikko KI (1995) Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 64:403–434

    Article  CAS  PubMed  Google Scholar 

  • Rapcsak M, Oganov VS, Szoor A, Skuratova SA, Szilagyi T, Takacs O (1983) Effect of weightlessness on the function of rat skeletal muscles on the biosatellite “Cosmos-1129”. Acta Physiol Hung 62:225–228

    CAS  PubMed  Google Scholar 

  • Reeves ND, Maganaris CN, Ferretti G, Narici MV (2002) Influence of simulated microgravity on human skeletal muscle architecture and function. J Gravit Physiol 9:P153–P154

    CAS  PubMed  Google Scholar 

  • Reeves ND, Maganaris CN, Ferretti G, Narici MV (2005) Influence of 90-day simulated microgravity on human tendon mechanical properties and the effect of resistive countermeasures. J Appl Physiol 98:2278–2286

    Article  CAS  PubMed  Google Scholar 

  • Rennie MJ, Selby A, Atherton P, Smith K, Kumar V, Glover EL, Philips SM (2010) Facts, noise and wishful thinking: muscle protein turnover in aging and human disuse atrophy. Scand J Med Sci Sports 20:5–9

    Google Scholar 

  • Riley DA, Bain JL, Thompson JL, Fitts RH, Widrick JJ, Trappe SW, Trappe TA, Costill DL (2000) Decreased thin filament density and length in human atrophic soleus muscle fibers after spaceflight. J Appl Physiol 88:567–572

    CAS  PubMed  Google Scholar 

  • Rittweger J, Felsenberg D, Maganaris C, Ferretti JL (2007) Vertical jump performance after 90 days bed rest with and without flywheel resistive exercise, including a 180 days follow-up. Eur J Appl Physiol 100:427–436

    Article  PubMed  Google Scholar 

  • Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ (2001) Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3:1009–1013

    Article  CAS  PubMed  Google Scholar 

  • Roy RR, Bello MA, Bouissou P, Edgerton VR (1987) Size and metabolic properties of fibers in rat fast-twitch muscles after hindlimb suspension. J Appl Physiol 62:2348–2357

    CAS  PubMed  Google Scholar 

  • Rozier CK, Elder JD, Brown M (1979) Prevention of atrophy by isometric exercise of a casted leg. J Sports Med Phys Fitness 19:191–194

    CAS  PubMed  Google Scholar 

  • Rudnick J, Puttmann B, Tesch PA, Alkner B, Schoser BG, Salanova M, Kirsch K, Gunga HC, Schiffl G, Luck G, Blottner D (2004) Differential expression of nitric oxide synthases (NOS 1-3) in human skeletal muscle following exercise countermeasure during 12 weeks of bed rest. FASEB J 18:1228–1230

    Google Scholar 

  • Rummel JA, Sawin CF, Michel EL, Buderer MC, Thornton WT (1975) Exercise and long duration spaceflight through 84 days. J Am Med Womens Assoc 30:173–187

    CAS  PubMed  Google Scholar 

  • Ryan AS, Dobrovolny CL, Smith GV, Silver KH, Macko RF (2002) Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil 83:1703–1707

    Article  PubMed  Google Scholar 

  • Sargeant AJ, Davies CT, Edwards RH, Maunder C, Young A (1977) Functional and structural changes after disuse of human muscle. Clin Sci Mol Med 52:337–342

    CAS  PubMed  Google Scholar 

  • Schulze K, Gallagher P, Trappe S (2002) Resistance training preserves skeletal muscle function during unloading in humans. Med Sci Sports Exerc 34:303–313

    Article  PubMed  Google Scholar 

  • Seynnes OR, Maffiuletti NA, Maganaris CN, de Boer MD, Pensini M, di Prampero PE, Narici MV (2008) Soleus T reflex modulation in response to spinal and tendinous adaptations to unilateral lower limb suspension in humans. Acta Physiol (Oxf) 194:239–251

    Article  CAS  Google Scholar 

  • Shackelford LC, LeBlanc AD, Driscoll TB, Evans HJ, Rianon NJ, Smith SM, Spector E, Feeback DL, Lai D (2004) Resistance exercise as a countermeasure to disuse-induced bone loss. J Appl Physiol 97:119–129

    Article  CAS  PubMed  Google Scholar 

  • Shyy JY, Chien S (1997) Role of integrins in cellular responses to mechanical stress and adhesion. Curr Opin Cell Biol 9:707–713

    Article  CAS  PubMed  Google Scholar 

  • Stevens L, Mounier Y, Holy X (1993) Functional adaptation of different rat skeletal muscles to weightlessness. Am J Physiol 264:R770–R776

    CAS  PubMed  Google Scholar 

  • Stewart CE (2004) The physiology of stem cells: potential for the elderly patient. J Musculoskelet Neuronal Interact 4:179–183

    CAS  PubMed  Google Scholar 

  • Suzuki Y, Kashihara H, Takenaka K, Kawakubo K, Makita Y, Goto S, Ikawa S, Gunji A (1994) Effects of daily mild supine exercise on physical performance after 20 days bed rest in young persons. Acta Astronaut 33:101–111

    Article  CAS  PubMed  Google Scholar 

  • Talmadge RJ (2000) Myosin heavy chain isoform expression following reduced neuromuscular activity: potential regulatory mechanisms. Muscle Nerve 23:661–679

    Article  CAS  PubMed  Google Scholar 

  • Templeton GH, Padalino M, Manton J, Glasberg M, Silver CJ, Silver P, DeMartino G, Leconey T, Klug G, Hagler H et al (1984) Influence of suspension hypokinesia on rat soleus muscle. J Appl Physiol 56:278–286

    CAS  PubMed  Google Scholar 

  • Tesch PA, Berg HE (1997) Resistance training in space. Int J Sports Med 18(Suppl 4):S322–S324

    Article  PubMed  Google Scholar 

  • Tesch PA, Trieschmann JT, Ekberg A (2004) Hypertrophy of chronically unloaded muscle subjected to resistance exercise. J Appl Physiol 96:1451–1458

    Article  CAS  PubMed  Google Scholar 

  • Tesch PA, Berg HE, Bring D, Evans HJ, LeBlanc AD (2005) Effects of 17-day spaceflight on knee extensor muscle function and size. Eur J Appl Physiol 93:463–468

    Article  PubMed  Google Scholar 

  • Thom JM, Thompson MW, Ruell PA, Bryant GJ, Fonda JS, Harmer AR, De Jonge XA, Hunter SK (2001) Effect of 10-day cast immobilization on sarcoplasmic reticulum calcium regulation in humans. Acta Physiol Scand 172:141–147

    Article  CAS  PubMed  Google Scholar 

  • Thomason DB, Booth FW (1990) Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68:1–12

    Article  CAS  PubMed  Google Scholar 

  • Thorton WE, Rummel JA (1977) Muscular deconditioning and its prevention in space flight. In: Johnson RS, Deitlein LF (eds) Biomedical results from skylab. NASA, Washington, DC, pp 191–197

    Google Scholar 

  • Trappe SW, Trappe TA, Lee GA, Widrick JJ, Costill DL, Fitts RH (2001) Comparison of a space shuttle flight (STS-78) and bed rest on human muscle function. J Appl Physiol 91:57–64

    CAS  PubMed  Google Scholar 

  • Trappe S, Trappe T, Gallagher P, Harber M, Alkner B, Tesch P (2004) Human single muscle fibre function with 84 day bed-rest and resistance exercise. J Physiol 557:501–513

    Article  CAS  PubMed  Google Scholar 

  • Trappe TA, Burd NA, Louis ES, Lee GA, Trappe SW (2007) Influence of concurrent exercise or nutrition countermeasures on thigh and calf muscle size and function during 60 days of bed rest in women. Acta Physiol (Oxf) 191:147–159

    Article  CAS  Google Scholar 

  • Urban RJ, Bodenburg YH, Gilkison C, Foxworth J, Coggan AR, Wolfe RR, Ferrando A (1995) Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am J Physiol 269:E820–E826

    CAS  PubMed  Google Scholar 

  • Veldhuizen JW, Verstappen FT, Vroemen JP, Kuipers H, Greep JM (1993) Functional and morphological adaptations following four weeks of knee immobilization. Int J Sports Med 14:283–287

    Article  CAS  PubMed  Google Scholar 

  • Wade CE, Stanford KI, Stein TP, Greenleaf JE (2005) Intensive exercise training suppresses testosterone during bed rest. J Appl Physiol 99:59–63

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Casaburi R, Taylor WE, Aboellail H, Storer TW, Kopple JD (2005) Skeletal muscle mRNA for IGF-IEa, IGF-II, and IGF-I receptor is decreased in sedentary chronic hemodialysis patients. Kidney Int 68:352–361

    Article  CAS  PubMed  Google Scholar 

  • White MJ, Davies CT, Brooksby P (1984) The effects of short-term voluntary immobilization on the contractile properties of the human triceps surae. Q J Exp Physiol 69:685–691

    CAS  PubMed  Google Scholar 

  • Widrick JJ, Romatowski JG, Bain JL, Trappe SW, Trappe TA, Thompson JL, Costill DL, Riley DA, Fitts RH (1997) Effect of 17 days of bed rest on peak isometric force and unloaded shortening velocity of human soleus fibers. Am J Physiol 273:C1690–C1699

    CAS  PubMed  Google Scholar 

  • Widrick JJ, Knuth ST, Norenberg KM, Romatowski JG, Bain JL, Riley DA, Karhanek M, Trappe SW, Trappe TA, Costill DL, Fitts RH (1999) Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres. J Physiol 516(Pt 3):915–930

    Article  CAS  PubMed  Google Scholar 

  • Widrick JJ, Trappe SW, Romatowski JG, Riley DA, Costill DL, Fitts RH (2002) Unilateral lower limb suspension does not mimic bed rest or spaceflight effects on human muscle fiber function. J Appl Physiol 93:354–360

    CAS  PubMed  Google Scholar 

  • Wilkie DR (1949) The relation between force and velocity in human muscle. J Physiol 110:249–280

    CAS  PubMed  Google Scholar 

  • Wineski LE, von Deutsch DA, Abukhalaf IK, Pitts SA, Potter DE, Paulsen DF (2002) Muscle-specific effects of hindlimb suspension and clenbuterol in mature male rats. Cells Tissues Organs 171:188–198

    Article  CAS  PubMed  Google Scholar 

  • Yamashita-Goto K, Okuyama R, Honda M, Kawasaki K, Fujita K, Yamada T, Nonaka I, Ohira Y, Yoshioka T (2001) Maximal and submaximal forces of slow fibers in human soleus after bed rest. J Appl Physiol 91:417–424

    CAS  PubMed  Google Scholar 

  • Yoshida N, Sairyo K, Sasa T, Fukunaga M, Koga K, Ikata T, Yasui N (2003) Electrical stimulation prevents deterioration of the oxidative capacity of disuse-atrophied muscles in rats. Aviat Space Environ Med 74:207–211

    CAS  PubMed  Google Scholar 

  • Zachwieja JJ, Smith SR, Lovejoy JC, Rood JC, Windhauser MM, Bray GA (1999) Testosterone administration preserves protein balance but not muscle strength during 28 days of bed rest. J Clin Endocrinol Metab 84:207–212

    Article  CAS  PubMed  Google Scholar 

  • Zange J, Muller K, Schuber M, Wackerhage H, Hoffmann U, Gunther RW, Adam G, Neuerburg JM, Sinitsyn VE, Bacharev AO, Belichenko OI (1997) Changes in calf muscle performance, energy metabolism, and muscle volume caused by long-term stay on space station MIR. Int J Sports Med 18(Suppl 4):S308–S309

    Article  PubMed  Google Scholar 

  • Zimmers TA, Davies MV, Koniaris LG, Haynes P, Esquela AF, Tomkinson KN, McPherron AC, Wolfman NM, Lee SJ (2002) Induction of cachexia in mice by systemically administered myostatin. Science 296:1486–1488

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

A significant portion of this Review paper makes direct reference to published literature of Prof. PE di Prampero and co-workers and indirectly, to work performed through the close and most enjoyable collaboration we shared over the last 30 years. We are also grateful to the funding agencies that partly supported this work (ESA, ASI and the Slovenian Ministry of Defence) and to Prof. Rado Pisot (University of Primorska, Science and Research Centre Koper, Institute for Kinesiology Research, Slovenia) for creating the opportunity for performing some of the ground-based studies cited in this paper.

Author information

Authors and Affiliations

  1. Institute for Biomedical Research into Human Movement and Health, Faculty of Science and Engineering, Manchester Metropolitan University, John Dalton Building, Chester Street, Manchester, M1 5GD, UK

    M. V. Narici

  2. Division of Applied Medicine, School of Medicine and Dentistry, University of Aberdeen, Scotland, UK

    M. D. de Boer

Authors
  1. M. V. Narici
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. D. de Boer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. V. Narici.

Additional information

Communicated by Susan Ward.

This article is published as part of the Special Issue dedicated to Pietro di Prampero, formerly Editor-in-Chief of EJAP.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Narici, M.V., de Boer, M.D. Disuse of the musculo-skeletal system in space and on earth. Eur J Appl Physiol 111, 403–420 (2011). https://doi.org/10.1007/s00421-010-1556-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-010-1556-x

Keywords

Search

Navigation